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Animal Behavior 64:697-708 ANIMAL BEHAVIOUR, 2002, 64, 697–708 doi:10.1006/anbe.2002.4011, available online at http://www.idealibrary.com on Spatiotemporal patterns of intraspecific aggression in the invasive Argentine ant ANDREW V. SUAREZ*‡, DAVID A. HOLWAY*, DANGSHENG LIANG†, NEIL D. TSUTSUI*‡ & TED J. CASE* *Division of Biological Sciences, Section of Ecology, Behavior & Evolution, University of California San Diego †Clorox Technical Center, Pleasanton, California, U.S.A. ‡Center for Population Biology, Section of Ecology & Evolution, University of California Davis (Received 29 August 2001; initial acceptance 9 November 2001; final acceptance 3 April 2002; MS. number: A9148) The Argentine ant, Linepithema humile, is a widespread invasive species characterized by reduced intraspecific aggression within introduced populations. To illuminate the mechanisms underlying nestmate recognition in Argentine ants, we studied the spatial and temporal fidelity of intraspecific aggression in an introduced population of Argentine ants within which intraspecific aggression does occur. We quantified variation in the presence or absence of intraspecific aggression among nests over time both in the field and under controlled laboratory conditions to gain insight into the role of environmental factors as determinants of nestmate discriminatory ability. In addition, we compared levels of intraspecific aggression between nest pairs to the similarity of their cuticular hydrocarbons to determine the potential role of these compounds as labels for nestmate discrimination. In both field and laboratory comparisons, nest pairs behaved in a consistent manner throughout the course of the experiment: pairs that fought did so for an entire year, and pairs that did not fight remained nonaggressive. Moreover, we found a negative relationship between cuticular hydrocarbon similarity and the degree of aggression between nests, suggesting that these hydrocarbons play a role in nestmate discriminatory ability. In contrast to the prevailing pattern, ants from one site showed a marked change in behaviour during the course of this study. A concomitant change was also seen in the cuticular hydrocarbon profiles of ants from this site. 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved. In social insects, systems for nestmate recognition are in ants (Breed & Bennett 1987; Ho¨lldobler & often well developed, allowing colony boundaries to be Wilson 1990; Banschbach & Herbers 1996; Beye maintained with high fidelity. Because social insect et al. 1998; Stuart & Herbers 2000). colonies are typically groups of related individuals, non- Many insects use cuticular hydrocarbons to recognize reproductives gain inclusive fitness by preferentially help- mates, conspecifics and colony members (Howard & ing nestmates (Hamilton 1964). Cues used to distinguish Blomquist 1982; Vander Meer & Morel 1998). As a result, nestmates from non-nestmates may be environmentally variation in cuticular hydrocarbons has been used to derived, innate (genetically based), or a combination of identify species (Howard et al. 1982; Vander Meer & both. Using these cues, individuals can discriminate nest- Lofgren 1990), to differentiate populations (Nowbahari mates from non-nestmates, and thus accept or reject et al. 1990), and to distinguish among different individuals they encounter. Environmental odours, such castes within social insect colonies (Howard et al. 1982; as those acquired from food or nesting material, can be Haverty et al. 1996). Intercolonial aggression in ants used to assess group membership in many wasps, bees, also correlates with variation in cuticular hydrocarbon termites, and some ants (Ho¨lldobler & Michener 1980; profiles (Bonavita-Cougourdan et al. 1987; Nowbahari Gamboa et al. 1986; Carlin 1989; Ho¨lldobler & Wilson et al. 1990). Moreover, recent experiments suggest 1990; Breed 1998). Current evidence suggests that that cuticular hydrocarbons directly affect nestmate genetically based systems are also important, particularly recognition in some ant species (Lahav et al. 1999; Thomas et al. 1999; Boulay et al. 2000; Liang & Silverman Correspondence and present address: A. V. Suarez, University of California, Department of Environmental Science, Policy and 2000). Management, Division of Insect Biology, 201 Wellman Hall #3112, Because ants show a variety of colony structures, they Berkeley, CA 94720-3112, U.S.A. (email: [email protected]. have long been used as model organisms to examine the edu). mechanisms underlying recognition systems (Carlin & 697 0003–3472/02/$35.00/0 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved. 698 ANIMAL BEHAVIOUR, 64, 5 Ho¨lldobler 1986; Ho¨lldobler & Wilson 1990). In many In this paper, we examined the temporal fidelity of ants, nestmate discrimination is well developed and nestmate recognition among nests of Argentine ants that workers aggressively defend territories, particularly vary in the degree to which they show intraspecific against conspecifics, resulting in a form of colony struc- aggression. We studied changes in behaviour among ture known as multicoloniality (Ho¨lldobler & Wilson nests over time in the field and under controlled 1977). In contrast, some species show a colony structure laboratory conditions in order to gain insight into the known as unicoloniality in which levels of intraspecific role of environmental factors as determinants of nest- aggression are reduced or absent and colony boundaries mate discriminatory ability. In addition, we compared are weak to nonexistent (Ho¨lldobler & Wilson 1977). levels of intraspecific aggression between nest pairs to the Unicoloniality is rare in ants, and is most commonly similarity of their cuticular hydrocarbons to investigate observed in mound-building wood ants (of the Formica their potential role in nestmate discrimination. rufa group) and many invasive ants, including the Argentine ant, Linepithema humile (Ho¨lldobler & Wilson 1990; Passera 1994; Bourke & Franks 1995). METHODS Native to South America, Argentine ants have become established in Mediterranean and subtropical climates Selection of Field Sites throughout the world (Suarez et al. 2001; Tsutsui et al. 2001) where they commonly displace native ants (Bond To investigate temporal variation in nestmate discrimi- & Slingsby 1984; Ward 1987; Cammell et al 1996; natory ability in the Argentine ant, we identified nine Human & Gordon 1996; Holway 1998; Suarez et al. invaded sites in southern California that varied in the 1998). Within native populations, Argentine ants typi- degree to which Argentine ants showed intraspecific cally appear more multicolonial, with intraspecific aggression. Because intraspecific aggression is rare in the aggression frequently occurring over short (<100 m) introduced range, extensive surveys throughout southern spatial scales (Suarez et al. 1999; Tsutsui et al. 2000). California were conducted between 1997 and 1999 to Within introduced populations, however, intraspecific identify colonies among which intraspecific aggression aggression is almost entirely absent and Argentine ants occurred (Fig. 1; Suarez et al. 1999; Tsutsui et al. 2000). form expansive supercolonies (Newell & Barber 1913; Colonies from most of these locations have been used Markin 1968; Ho¨lldobler & Wilson 1990; Wayetal. previously to investigate the genetic correlates (Tsutsui 1997; Suarez et al. 1999; Tsutsui et al. 2000; Giraud et al. 2000) and colony-level consequences (Holway et al. et al. 2002). It has been suggested that unicolonialty has 1998) of intraspecific aggression. In August 1999, we arisen in introduced populations of the Argentine ant as collected workers from one nest at each of nine sites and a result of reduced genetic diversity following their performed pairwise behavioural assays between workers introduction (Tsutsui et al. 2000). Introduced popula- from all the sites (N=36 nest pairs). In addition, we tions may not possess the levels of genetic diversity collected workers, brood and queens from eight sites to necessary to distinguish nestmates from non-nestmates. establish laboratory colonies. Each month for 12 months, This variation in colony structure may also underlie the we returned to each site of collection and repeated Argentine’s ability to displace native species. Specifi- behavioural assays among all nest pairs. cally, the numerical advantages key to the Argentine ant’s success in displacing native species (Holway 1999; Holway & Case 2001) may result from the reduced Maintenance of Laboratory Colonies mortality, higher foraging rates and greater brood pro- duction resulting from an abandonment of costly We established laboratory colonies of Argentine ants intraspecific territorial defence (Holway et al. 1998). from the eight field nests in August 1999, following the Given the lack of intraspecific aggression typical of protocol of Holway et al. (1998). Each colony occupied a introduced populations of Argentine ants, and its plastic nest container (30148 cm) lined with Fluon potential role in their success, it is of great interest to (Northern Products Inc., Woonsocket, Rhode Island, determine the mechanisms responsible for nestmate U.S.A.) and Tanglefoot (The Tanglefoot Company, recognition in this species. Recent work on Argentine Grand Rapids, Michigan, U.S.A.) to prevent ants from ants found a negative relationship between the extent escaping. Each nest container held three test-tubes half-
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